Re-shaping spurge pioneers : circumscription,
taxonomy and phylogeny of Mallotus (Euphorbiaceae
s.s.)
Sierra Daza, S.E.C.
Citation
Sierra Daza, S. E. C. (2007, September 11). Re-shaping spurge pioneers : circumscription, taxonomy and phylogeny of Mallotus (Euphorbiaceae s.s.). Retrieved from https://hdl.handle.net/1887/12308
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GENERAL INTRODUCTION
In this thesis the results of morphological and phylogenetic studies on the genus Mallotus Lour. are presented. The aims of these studies were to revise part of the Malesian Mallotus species, to study their phylogeny, and to evaluate the current classification and the characters used to support it. Euphorbiaceae s.s. and Mallotus will be introduced briefly and the research questions and methodology will be presented in detail. This introduction is concluded with an outline of the thesis.
EUPHORBIACEAE
The Euphorbiaceae or spurge family was first described and treated by De Jussieu (1823, 1824). Until recently there existed a broad circumscription of the family (Euphorbiaceae s.l.). The latest classification of the Euphorbiaceae s.l., proposed by Webster (1975, 1994a, 1994b) and updated by Radcliffe-Smith (2001), comprised five subfamilies, c.
340 genera, and c. 9000 species. However, because of the morphological heterogeneity of its members the circumscription of the family has long been problematic. This is reflected in the variety of intra-familiar classifications that have been proposed:
Corner 1976, Webster 1987, Meeuse 1990, Huber 1991, Sutter & Endress 1995. Recent molecular phylogenies, however, have provided new insights into the Euphorbiaceae s.l.
Chase et al. (1993) first showed that the Euphorbiaceae s.l. might not be monophyletic, which was later confirmed with a better taxon sampling and more data (Wurdack &
Chase, 1996; Soltis et al., 1997, 2000; Savolainen et al., 2000a, 2000b; Chase et al., 2002; Wurdack, 2002; Davis & Chase, 2004; Davis & Wurdack, 2004). Following the APG II (2003), the Euphorbiaceae s.l. are now divided into five families: Euphorbiaceae s.s., Pandaceae, Phyllanthaceae, Picrodendraceae and Putranjivaceae; all placed in the order Malpighiales. However, the relationships among them still is unclear and needs further research (Davis et al., 2005; Tokuoka & Tobe, 2006). The breaking up of the Euphorbiaceae s.l. has resulted in three biovulate and two uniovulate families (this division based on the number of ovules was already proposed by De Jussieu in 1823, 1824).
The Euphorbiaceae s.s. is composed of the former subfamilies Crotonoideae, Euphorbioideae and part of the Acalyphoideae, all possessing a single ovule per locule. Molecular phylogenetic studies by Wurdack et al. (2005) on the Euphiorbiaceae s.s., recognize seven major lineages, and two new subfamilies, the Peroideae and Cheilosoideae, which are successive sisters to the remainder Euphorbiaceae s.s.
Recently, Tokuoka (in press) presented a molecular phylogenetic analysis of Euphorbiaceae s.s. which confirmed the results of Wurdack et al. (2005), indicating that a palisadal exotegmen is a possible synapomorphy for all the Euphorbiaceae, except for the subfamily Peroideae. The family presently consists of 245 pantropical genera
Re-shaping spurge pioneers — Chapter 14 General Introduction 5
and c. 6300 species (based on estimates by Wurdack et al., 2005). A recent molecular phylogenetic study (Davis et al., 2007) suggests that the Euphorbiaceae s.s. should also include the Rafflesiaceae, as this family was found to be nested within Euphorbiaceae s.s. with strong support (94% bootstrap support, 1.0 Bayesian posterior probability).
However, from a morphological point of view both groups are very different. The Rafflesiaceae are leafless, stemless and rootless parasites with flowers up to a meter in diameter, while the Euphorbiaceae s.s. have different features than the above mentioned.
More important, and morphologically always deemed extremely important is the difference in number and position of the locules. In the Rafflesiaceae there are many ovules in an inferior ovary, while the spurges s.s. have a single ovule per locule and a superior ovary. Davies et al. (2007) suggest that the morphological restriction of the Rafflesiaceae prevents a clear identification of synapomorphies for both groups.
Not much is known about the origin of the Euphorbiaceae s.s. Molecular clock dating suggests a Cretaceous-late Aptian (c. 119.4 to 101.1 Ma) divergence of the family, while the few known fossils assigned to Euphorbiaceae s.s. indicate an Eocene (c. 56 to 34 Ma) diversification (Webster, 1967; Muller, 1981, Crepet & Daghlian, 1982;
Friis & Crepet, 1987; Dilcher & Manchester, 1988; Wikstrom et al., 2001; Davis et al., 2005).
Several species are known and cultivated for their economic value: Manihot esculenta Crantz is cultivated as an annual crop in tropical and subtropical regions as a major source for carbohydrates (manioc, cassava, yuca, tapioca); Hevea brasiliensis (Willd.
ex A.Juss.) Müll.Arg. (Para rubber tree) is the major commercial source of natural latex used to create rubber and chewing gum; Ricinus communis L. is cultivated to produce the highly valuable castor oil, which because of its unusual composition and chemistry is used in the manufacturing of soaps, lubricants, brake fluids, paints, plastics, perfumes, etc.; Aleurites moluccana L. (Willd.) is an indispensable spice in Indonesian cuisine, mainly acting as an enhancer (the raw seed is slightly poisonous, acting as a laxative);
the fatty seed oil is used industrially, also for illumination and medicinally (candle nut tree or Kemiri nut); Vernicia Lour. and Euphorbia L. species are used in the production of waxes, oil and vanish; Acalypha L., Codiaeum Rumph. ex A.Juss., Euphorbia L. and Ricinus L. species are widely cultivated as ornamentals; and the crushed leaves and stems of Croton setigerus Hook. (Fish weed) are known to be used as fish-stupefying poison. After Mabberley (1997), Siemonsma (1999), Kalkman (2003).
The Euphorbiaceae in the broad or strict sense are still a very large group and it is challenging to give a complete overview of the research done on these groups. Therefore, the following paragraph is limited to the Euphorbiaceae s.l. research performed at the Nationaal Herbarium Nederland (NHN) in recent years. At the NHN Universiteit Leiden branch, part of the plant systematic research has focused on the completion of the Flora of the Malesian region (Brunei, Indonesia, Malaysia, the Philippines, Papua New Guinea, Singapore and Timor-Leste). In the beginning of the 1990’s a start was made with the treatment of the Euphorbiaceae s.l. for this Flora, which was based on the extensive work done by Airy Shaw. Since the start, several projects have been carried out, among others: Clonostylis S. Moore, Homonoia Lour., Ricinus L., Spathiostemon Blume, Wetria (Van Welzen, 1998); Lasiococca Hook.f. (Van Welzen, 1998, Van Welzen
& Sierra, 2005); Aleurites J.R.Forst. & G.Forst., Reutealis Airy Shaw, Vernicia Lour.
(Stuppy et al, 1999); Balakata Esser, Microstachys A.Juss., Shirakiopsis Esser, Stillingia
Garden ex L., Triadica Lour. (Esser, 1999); Baccaurea Lour. (Haegens, 2000); Aporosa Blume (Schot, 2004); Cleidion Blume (Kulju & Van Welzen, 2005); Antidesma Burm.
ex L. (Hoffmann, 2006).
During the last few years Mallotus has been the topic of several research projects, mainly because of the ecological importance of the genus in the tropical forests of Southeast Asia and its large number of species, viz. on ecology (Slik et al., 2003a; Slik, 2005); on leaf anatomy (Fišer et al., in prep.); on molecular phylogeny (Kulju et al., in press); on palynology (Chapters 5 & 6), and on macromorphology (Bollendorff et al., 2000; Slik & Van Welzen, 2001; Chapter 2; Chapter 3; Van Welzen & Sierra, 2005;
Chapter 4; Van Welzen et al., 2006; Van Welzen & Sierra, 2006; Chapter 5; Chapter 6;
Kulju et al., 2007; Van Welzen et al., in press).
MALLOTUS
Mallotus and its sister genus Macaranga, are good indicators of forest disturbance (Slik et al., 2003a). Mallotus shows a large variety of life-histories, some species being extreme pioneers, and others being climax species. Slik (2005) developed a methodology to assess the type of forest disturbance in lowland tropical forest in Borneo, in particular useful when ecological field data or historical records on disturbance are absent (http:
//www.nationaalherbarium.nl/macmalborneo/index.htm). For this purpose, ecological attributes in both genera were used together with three morphological characters related to the successional life history strategy of the species (wood density, seed size and leaf shape).
In Mallotus and Macaranga some species are also characterized by the presence of ants. For Macaranga several studies have been conducted to investigate the relationships with ants (Fiala et al., 1994, 1999; Federle et al., 1997; Itioka et al., 2000; Davies et al., 2001; Feldhaar et al., 2000, 2003) and some sections comprise species which are obligatory myrmecophytes (Blattner et al., 2001; Davies, 2001). In Mallotus this kind of strict relationship was not found. The role of the ants is possibly related to anti-herbivory defense mechanisms. In both genera the ants are apparently attracted by nectar secreted from sugar producing organs outside the flowers, the so-called extrafloral nectaries (So, 2004). In the non-obligatory myrmecophytes opportunistic ants visit the plants, killing competing insects and keeping competing plants, especially lianas at bay.
The genus Mallotus was described by De Loureiro in 1790. In the classifications of the Euphorbiaceae (Webster 1994; Radcliffe-Smith 2001) it was placed in the subtribe Rottlerinae together with seven or eight small genera. In the molecular phylogeny by Wurdack et al. (2005), using plastid rbcL and trnL-F, it is part of the core acalyphoid subclade A1. The large number of species in Mallotus together with their variable morphology has resulted in three main subgeneric classifications by Müller (1865, 1866), Pax & Hoffman (1914) and Airy Shaw (1968). The first was proposed by Müller Argoviensis (1865, 1866), recognizing a total of five sections (several are now separate genera). However, he classified some species which are now considered synonyms in different sections. This shows the large morphological variability within some of the species and also his unclear sectional delimitations. Pax & Hoffmann (1914) proposed a new subdivision into ten sections, which was later reduced to eight sections by Airy Shaw (1968): Axenfeldia (Baill.) Pax & K.Hoffm., Hancea Pax & K.Hoffm.,
Re-shaping spurge pioneers — Chapter 16 General Introduction 7
Mallotus Airy Shaw, Oliganthae Airy Shaw, Polyadenii Pax & K.Hoffm., Rottlera (Willd.) Rchb.f. & Zoll., Rottleropsis Müll.Arg., and Stylanthus (Rchb.f. & Zoll.) Pax
& K.Hoffm.
Two phylogenetic studies have specifically investigated the relationship between Mallotus and related genera. An analysis based on morphological data suggested that Mallotus sections Hancea and Oliganthae are not part of the main Mallotus clade, and that Mallotus and Macaranga are closely related (Slik & Van Welzen, 2001).
A molecular phylogenetic study using nuclear and plastid markers and with a far more comprehensive taxon sampling (including all but one of the Rottlerinae genera, and c. 24% of Mallotus species) further clarified the boundaries of Mallotus and its relationships with other genera (Kulju et al., 2007). This study confirmed the exclusion of the sections Hancea and Oliganthae. These sections form a clade together with the Rottlerinae genera Deuteromallotus and Cordemoya Baill., and are separated with strong support from the main Mallotus clade. Additionally, this study showed that the Mallotus clade is sister to a monophyletic Macaranga. The phylogeny of Kulju et al.
(in press) also confirmed the inclusion of Coccoceras in Mallotus, and demonstrated that Neotrewia Pax & K.Hoffm., Octospermum Airy Shaw and Trewia L., three mono- or ditypic Rottlerinae genera with atypically indehiscent fruits, are part of the main Mallotus clade. The three latter genera were subsequently included in Mallotus (Kulju et al., 2007). The two above mentioned phylogenetic analyses also studied the relationships within Mallotus s.s., and have tentatively shown some of the sections to be non-monophyletic. However, the analyses suffered from insufficient taxon sampling in the Mallotus s.s. clade, and from polytomies and low support in a large part of the resulting phylogenies. Thus, a study focusing on the phylogeny of Mallotus s.s. was clearly needed to evaluate the existing infrageneric classification by Airy Shaw (1968) and the importance and evolution of the morphological characters involved (Chapter 7).
Accompanying the inclusion of the genus Trewia (composed of two species) in Mallotus, Kulju & Van Welzen (in prep.) proposed the conservation of the name
‘Mallotus’ against Trewia. This was done to prevent numerous name changes, because Trewia, as an older name, would otherwise have a nomenclature priority over Mallotus.
The genus as presently circumscribed comprises c. 110 species and 5 sections. Most Mallotus species are shrubs or trees, and seldom climbers; most species are evergreen and only some deciduous. The species are predominantly dioecious, although a few species are dioecious and (rarely) monoecious. Typical features for Mallotus s.s. are the presence of fairly conspicuous, globose to disc-shaped glandular hairs (best seen on the lower leaf surface and inflorescences) and extrafloral nectaries on the upper leaf surface. Mallotus pollen is medium-sized (Polar axis by Equatorial diameter = 16—28.5 by 18—30.6 μm) and uniform in shape (3-(rarely 4-)colporate) and ornamentation (perforate/microreticulate with scabrae). For a review of diagnostic morphological features in Mallotus see Chapter 6 and for a generic description see Kulju et al.
(2007).
The genus has a palaeotropical distribution and is mainly found in (sub)tropical Asia and the West Pacific, with only two species in tropical Africa and Madagascar, M. oppositifolius (Geiseler) Müll.Arg. and M. subulatus Müll.Arg. respectively (for a map, see Kulju et al., 2007). In the Flora Malesiana region a total of 52 species are
recognized. They occur in different habitats, like the understorey of primary forest or in disturbed secondary forest, preferring open places. The plants also grow on a variety of soil types, and in wet and periodically inundated areas to well-drained soils. The species occur from sea level up to 2100 m altitude.
No exact age is known for the genus Mallotus. However, studies by García Massini
& Jacobs (2007) on megafloral composition and sedimentology in the Chilga region, North Western Ethiopian Plateau, based on well preserved fossils of leaves, suggest that the sister genus Macaranga was (at least) already present during the Late Oligocene (c. 27 Ma.).
RESEARCH QUESTIONS
This study is part of the Flora Malesiana project and, therefore, its main focus is the revision of the species of that region. However, we also studied non-Malesian species, in particular those from Thailand and Africa, to gain more knowledge about the morphological variation within the genus. Additionally the study of Thai taxa contributed to the ongoing work on the revision of the Euphorbiaceae for the Flora of Thailand.
The approach taken for the revisional work is to study the genus per section, following the traditional sectional delimitation of Airy Shaw (1968) based only on few characters:
leaves alternate or opposite, glandular hairs on the upper surface of leaf blade, leaf venation pinnate or triplinerved, presence or absence of a fenugreek smell in dried leaves, smooth or spiny fruits, and fruits densely covered with glandular hairs or not.
The main objective of this taxonomic study is to revise five sections of Mallotus in Malesia, Thailand and Africa, by establishing species delimitations based on morphology and to study their evolutionary relationships by addressing the following questions:
1) What are the circumscriptions of Mallotus sections Rottlera, Mallotus, Oliganthae, Axenfeldia and Rottleropsis and which species occur in the Flora Malesiana area, Thailand and Africa?
2) What are the species delimitations in these sections?
3) Are the sections as recognized monophyletic and what are the relationships among them?
4) What is the phylogenetic significance of macromorphological and leafanatomical characters in the delimitation of the sections and their relationships?
METHODOLOGY
The current infrageneric classification by Airy Shaw (1968) was used as a starting point for the revisional work. Three of the eight sections were recently revised, mainly for the Flora Malesiana area and Thailand (Polyadenii: Bollendorff et al., 2000; Hancea and Stylanthus: Slik & Van Welzen, 2001; Van Welzen et al., in press). The remaining five sections are revised in this thesis. For this purpose, dried plant specimens from different herbaria were asked on loan and used to study the morphological variability of the species within their whole distribution range.
Re-shaping spurge pioneers — Chapter 18 General Introduction 9
Blumeodendron Kurz, Cordemoya and Macaranga were used as outgroups for the phylogenetic analyses of Mallotus s.s., because they are closely related with Mallotus (Wurdack et al., 2005; Kulju et al. in press). A macromorphological dataset was gathered for 94 Mallotus species. For DNA sequence data (matK and gpd) only a subset of this sample (47–49 ingroup and 8 or 9 outgroup species, depending on the DNA region) was included. The sampling for leaf anatomical data corresponds in most parts with the one for DNA sequences. Specimens and the recent taxonomic revisions of Mallotus and Cordemoya in the Flora Malesiana area, Thailand and Africa were used as a source of information for constructing the morphological data matrix used in the phylogenetic analysis. For macromorphology, in total 38 qualitative characters (15 vegetative and 23 reproductive) and 18 quantitative characters (2 vegetative and 16 reproductive) were recorded. For leaf anatomy, in total 31 qualitative and 2 quantitative characters were gathered. For most quantitative data, discrete character states could not be defined due to overlap, therefore, two different coding methods were used that allowing overlap in the quantitative data: The gap-weighting method (Thiele, 1993; using MorphoCode v.1.0) and the ‘as such’ method using the program TNT (Goloboff et al., 2006) were used.
The robustness of a phylogeny can be tested by using different analytical methods (Huelsenbech & Rannala, 2003). In this study, the analyses were conducted with maximum parsimony (MP) and Bayesian inference (BI). MP uses the principle of parsimony as an optimality criterium to select among all possible evolutionary topologies. BI builds upon a likelihood principle and allows complex models of sequence evolution to be implemented (Holder & Lewis, 2003).
TNT v.1.1 (Goloboff et al., 2003a) was used for the MP analyses, treating polymor- phic characters as uncertainties. Most of the analyses were replicated with PAUP*
v.4.0b10 (Swofford, 2003), using Ratchet searches as implemented in PRAP v1.21 (Müller, 2004), which resulted in strict consensus cladograms identical to those found with the TNT analyses. Because conventional resampling support values (i.e., bootstrap and jackknife) can be distorted by non-equal weights in the dataset, the support was measured with symmetric resampling (SR). Bayesian inference (BI) of phylogeny with posterior probabilities (PP) was conducted with MrBayes v.3.1.2. The models of molecular evolution were selected using the Akaike Information Criterion (AIC) as implemented in MrModelTest v.2.2. Phylogenetic analyses were first conducted separately for three qualitative datasets (matK, gpd and morphology), and these results screened for hard incongruences (De Quiroz, 1993; Seelanan et al.,1997; Wiens, 1998).
The cutoff limit for hard incongruences was here set to SR 60 before they were combined in a single analysis of qualitative data. In the last phase, the quantitative morphological characters, either made discrete with the gap weighting method (Thiele, 1993), or coded
‘as such’ in TNT (Goloboff et al., 2006) were analyzed together with the qualitative data.
Because the taxon sample for the molecular data was much smaller than for the morphological data (see above), two sets of analyses were run for the combined datasets of molecular and morphological data: One with reduced taxon sampling, i.e., only including taxa with both molecular and morphological data, and a second one with full taxon sampling, i.e., including all possible taxa, but simultaneously introducing large amounts of missing data for the non-sequenced taxa. By performing total evidence
analyses the strength of the phylogenetic signal in a data set is usually increased (Johnson
& Soltis, 1998; Rokas et al., 2003; Wahlberg & Nylin, 2003).
The tracing of character evolution was performed with MacClade v4.08 (Maddison
& Maddison, 2001). For this purpose, all of the most parsimonious trees from the combined analyses including quantitative data and with full taxon sampling, were examined. While examining the synapomorphies for the clades, only unambiguous character changes were taken into account.
Species concept
The study presented in this thesis deals principally with the plant systematic revisional work of a number of different species in a particular genus. In practice this means that based on their phenotype, herbarium specimens are grouped together. These groups are then either associated with an existing type specimen, which is linked to a particular taxon name, or described as a new species. However, within this practice it is necessary to use a standardized species concept as a guide to decide whether a particular group of associated herbarium specimens constitutes a “true species” or not.
Here we opted for the morphological or typological species concept after Van Steenis (1957). This concept can be used in taxonomic revisions based on herbarium collections for comparison of morphological characters. It states that one should consider a particular group of associated herbarium specimens a different species from other groups/species, when it consistently differs in at least two independent morphological characters states. If there is only one morphological character state difference, then one should consider the specimens or groups, which are compared to belong to the same species. Arguably though, this one character state difference might warrant the recognition of different varieties (overlapping distribution area) or subspecies (difference in distribution area) within the species.
In subsequent studies using other sources of information these species can then be tested with other concepts given in literature like, among others, the Composite Species Concept (Kornet, 1993; Kornet & McAllister, 1993), the Phylogenetic Species Concept (Mayden, 1997).
OUTLINE OF THE THESIS
In Chapter 2 the revision of Mallotus sect. Rottlera in the Flora Malesiana area and Thailand is presented. This chapter pays special attention to the problems concerning the correct name of this section. Chapter 3 deals with Mallotus sect. Rottlera. It concerns the species Mallotus kongkandae, previously thought to be endemic to Thailand, and provides new insights concerning the present distribution of this species.
The revision of Mallotus sect. Mallotus is presented in Chapter 4. Only the spe- cies occurring in the Flora Malesiana area are treated here, because the species from Thailand have been dealt with separately outside (Van Welzen et al., in press).
Chapter 5 provides the revision of the monospecific Mallotus sect. Oliganthae. Based on a existing molecular phylogeny, using one plastid (trnL-F) and three nuclear (ITS, ncpGS, phyC) markers, a new circumscription of the monotypic genus Cordemoya, from the Mascarene Islands, including Mallotus sections Oliganthae and Hancea is proposed.
Re-shaping spurge pioneers — Chapter 110
Chapter 6 is the combined revision of Mallotus sections Axenfeldia and Rottleropsis, finalizing the revisional work in the Flora Malesiana area. Special attention is given to the problems concerning the delimitations of the two sections. The large number of species of the two sections is presented in regional keys and a synoptical key. Apart from species occurring in Malesia and Thailand, the only two African species in Mallotus, part of sect. Rottleropsis, are revised. Additionally, a general classification of the genus Mallotus is presented.
In chapter 7, several phylogenetic analyses are presented in order to obtain insights in the monophyly of and relationships among the six classical sections within Mallotus s.s. The resulting phylogenies are also used to study the significance of morphological characters for this infrageneric classification. The analyses are based on a combined macromorphological, leaf anatomical and molecular (matK, gpd) dataset. The mor- phological data also includes quantitative data that is analyzed using two different methods.
